Hierarchy of the genetic interactions that specify the anteroposterior segmentation pattern of the Drosophila embryo as monitored by caudal protein expression

The establishment of the body pattern of Drosophila along the anteroposterior axis requires the coordinated functions of at least three classes of genes. First, the maternally active coordinate genes define the polarity of the embryo and act as primary determinants; second, the segmentation genes divide the developing embryo into the correct number of segments and third, the segments become specified by the homeotic selector genes. We have examined the effects of mutations in the genes of the first two classes on the spatial distribution of the protein product(s) of the caudal (cad) gene, which in wild type shows a graded distribution along the anteroposterior axis during the syncytial blastoderm stage, whereas its persistent zygotic expression is confined to the telson region (the posterior terminal structures). Mutations in maternal genes that specify the spatial coordinates of the egg and the future embryo change the gradient distribution of cad according to the alterations of the fate map which they produce. A second group of maternally expressed genes, the gap genes of the ‘grandchildless-knirps’ group, which are considered to represent posterior activities, do not have any effect on the cad gradient. The same is true for the zygotic segmentation genes that are active after fertilization. However, the same class of zygotic genes partly affects the zygotic cad expression in the telson. Therefore, the two phases of cad expression represent different levels within the genetic hierarchy. The cad protein gradient seems to form in response to the primary maternal determinants independent of the segmentation genes, whereas the latter influence zygotic cad expression in the telson region which corresponds to a homeotic selector gene function.